A novel vasoactive peptide “PG1” from buffalo ice-cream protects from angiotensin-evoked high blood pressure

Antioxidants

Volumn 10, Issue 3, 2021, Pages 1-17

  Carrizzo, Albino ^a,b   Basilicata, Manuela Giovanna ^c   Pepe, Giacomo ^c   Sørensen, Kasper K ^d   Ciccarelli, Michele ^a   Di Sarno, Veronica ^c   Damato, Antonio ^b   Venturini, Eleonora ^b   Borrelli, Anna ^e   Musella, Simona ^f   Abate, Mario ^a   Di Pietro, Paola ^a   Ostacolo, Carmine ^g   Campiglia, Pietro ^c   Vecchione, Carmine ^a,b  

^a UNIVERSITY OF SALERNO   (Italy)

^b IRCCS NEUROMED   (Italy)

^c UNIVERSITY OF SALERNO   (Italy)

^d UNIVERSITY OF COPENHAGEN   (Denmark)

^e UNIVERSITY HOSPITAL SAN GIOVANNI DI DIO E RUGGI D ARAGONA   (Italy)

^f European Biomedical Research Institute of Salerno   (Italy)

^g UNIVERSITY OF NAPLES FEDERICO II   (Italy)

Author keywords

Angiotensin II; Cardiovascular; Natural derived peptide

Indexed keywords

EID: 85102255822     PISSN: None     EISSN: 20763921     Source Type: Journal    
DOI: 10.3390/antiox10030441     Document Type: Article

References (52)

1. Weycker, D.; Nichols, G.A.; O’Keeffe-Rosetti, M.; Edelsberg, J.; Khan, Z.M.; Kaura, S.; Oster, G. Risk-Factor Clustering and Cardiovascular Disease Risk in Hypertensive Patients. Am. J. Hypertens. 2007, 20, 599–607. [CrossRef]
2. Touyz, R.M. Reactive oxygen species, vascular oxidative stress, and redox signaling in hypertension: What is the clinical significance? Hypertension 2004, 44, 248–252. [CrossRef] [PubMed]
3. Touyz, R.M. Intracellular mechanisms involved in vascular remodelling of resistance arteries in hypertension: Role of angiotensin II. Exp Physiol. 2005, 90, 449–455. [CrossRef] [PubMed]
4. Harvey, A.; Montezano, A.C.; Lopes, R.A.; Rios, F.; Touyz, R.M. Vascular Fibrosis in Aging and Hypertension: Molecular Mechanisms and Clinical Implications. Can. J. Cardiol. 2016, 32, 659–668. [CrossRef]
5. Carrizzo, A.; Forte, M.; Lembo, M.; Formisano, L.; Puca, A.A.; Vecchione, C. Rac-1 as a new therapeutic target in cerebro-and cardio-vascular diseases. Curr. Drug Targets 2014, 15, 1231–1246. [CrossRef]
6. Drummond, G.R.; Sobey, C.G. Endothelial NADPH oxidases: Which NOX to target in vascular disease? Trends Endocrinol. Metab. 2014, 25, 452–463. [CrossRef]
7. Sedeek, M.; Nasrallah, R.; Touyz, R.M.; Hebert, R.L. NADPH oxidases, reactive oxygen species, and the kidney: Friend and foe. J. Am. Soc. Nephrol. 2013, 24, 1512–1518. [CrossRef]
8. Burtenshaw, D.; Hakimjavadi, R.; Redmond, E.M.; Cahill, P.A. Nox, Reactive Oxygen Species and Regulation of Vascular Cell Fate. Antioxidants 2017, 6, 90. [CrossRef] [PubMed]
9. Zafari, A.M.; Ushio-Fukai, M.; Akers, M.; Yin, Q.; Shah, A.; Harrison, D.G.; Taylor, W.R.; Griendling, K.K. Role of NADH/NADPH oxidase-derived H2O2 in angiotensin II-induced vascular hypertrophy. Hypertension 1998, 32, 488–495. [CrossRef] [PubMed]
10. Vecchione, C.; Patrucco, E.; Marino, G.; Barberis, L.; Poulet, R.; Aretini, A.; Maffei, A.; Gentile, M.T.; Storto, M.; Azzolino, O.; et al. Protection from angiotensin II-mediated vasculotoxic and hypertensive response in mice lacking PI3Kgamma. J. Exp. Med. 2005, 201, 1217–1228. [CrossRef]
11. Williams, B.; Mancia, G.; Spiering, W.; Rosei, E.A.; Azizi, M.; Burnier, M.; Clement, D.L.; Coca, A.; de Simone, G.; Dominiczak, A.; et al. 2018 ESC/ESH Guidelines for the management of arterial hypertension. Eur. Heart J. 2018, 39, 3021–3104. [CrossRef] [PubMed]
12. Ives, C.W.; Oparil, S. What is the first choice for blood pressure treatment? Lancet 2019, 394, 1782–1784. [CrossRef]
13. Carrizzo, A.; Izzo, C.; Forte, M.; Sommella, E.; Di Pietro, P.; Venturini, E.; Ciccarelli, M.; Galasso, G.; Rubattu, S.; Campiglia, P.; et al. A Novel Promising Frontier for Human Health: The Beneficial Effects of Nutraceuticals in Cardiovascular Diseases. Int. J. Mol. Sci. 2020, 21, 8706. [CrossRef] [PubMed]
14. Cicero, A.F.G.; Colletti, A. An update on the safety of nutraceuticals and effects on lipid parameters. Expert Opin. Drug Saf. 2018, 17, 303–313. [CrossRef] [PubMed]
15. Dima, C.; Assadpour, E.; Dima, S.; Jafari, S.M. Bioavailability of nutraceuticals: Role of the food matrix, processing conditions, the gastrointestinal tract, and nanodelivery systems. Compr. Rev. Food Sci. Food Saf. 2020, 19, 954–994. [CrossRef] [PubMed]
16. Carrizzo, A.; Conte, G.M.; Sommella, E.; Damato, A.; Ambrosio, M.; Sala, M.; Scala, M.C.; Aquino, R.P.; De Lucia, M.; Madonna, M.; et al. Novel Potent Decameric Peptide of Spirulina platensis Reduces Blood Pressure Levels Through a PI3K/AKT/eNOS-Dependent Mechanism. Hypertension 2019, 73, 449–457. [CrossRef] [PubMed]
17. Drevet, P. Evidence of antihypertensive effect of a land snail (Helix aspersa) by-product hydrolysate-Identification of involved peptides. Ann. Cardiol. Angeiol. 2017, 66, 140–148. [CrossRef]
18. Dabarera, M.C.; Athiththan, L.V.; Perera, R.P. Antihypertensive peptides from curd. Int. Q. J. Res. 2015, 36, 214–219. [CrossRef] [PubMed]
19. McGregor, R.A.; Poppitt, S.D. Milk protein for improved metabolic health: A review of the evidence. Nutr. Metab. 2013, 10, 46. [CrossRef] [PubMed]
20. Pepe, G.; Pagano, F.; Adesso, S.; Sommella, E.; Ostacolo, C.; Manfra, M.; Chieppa, M.; Sala, M.; Russo, M.; Marzocco, S.; et al. Bioavailable Citrus sinensis extract: Polyphenolic composition and biological activity. Molecules 2017, 22, 623. [CrossRef]
21. Chan, C.O.; Jing, J.; Xiao, W.; Tan, Z.X.; Lv, Q.Y.; Yang, J.Y.; Chen, S.B. Enhanced Intestinal Permeability of Bufalin by a Novel Bufalin-Peptide-Dendrimer Inclusion through Caco-2 Cell Monolayer. Molecules 2017, 22, 2088. [CrossRef] [PubMed]
22. Hubatsch, I.; Ragnarsson, E.G.E.; Artursson, P. Determination of drug permeability and prediction of drug absorption in Caco-2 monolayers. Nat. Protoc. 2007, 2, 2111–2119. [CrossRef]
23. Ranieri, R.; Ciaglia, E.; Amodio, G.; Picardi, P.; Proto, M.C.; Gazzerro, P.; Laezza, C.; Remondelli, P.; Bifulco, M.; Pisanti, S. N6-isopentenyladenosine dual targeting of AMPK and Rab7 prenylation inhibits melanoma growth through the impairment of autophagic flux. Cell Death Differ. 2018, 25, 353–367. [CrossRef] [PubMed]
24. Carrizzo, A.; Moltedo, O.; Damato, A.; Martinello, K.; Di Pietro, P.; Oliveti, M.; Acernese, F.; Giugliano, G.; Izzo, R.; Sommella, E.; et al. New Nutraceutical Combination Reduces Blood Pressure and Improves Exercise Capacity in Hypertensive Patients Via a Nitric Oxide-Dependent Mechanism. J. Am. Heart. Assoc. 2020, 9, e014923. [CrossRef] [PubMed]
25. Persico, M.; Masarone, M.; Damato, A.; Ambrosio, M.; Federico, A.; Rosato, V.; Bucci, T.; Carrizzo, A.; Vecchione, C. Non alcoholic fatty liver disease and eNOS dysfunction in humans. BMC Gastroenterol. 2017, 17, 35. [CrossRef]
26. Huang, H.; Rabenstein, D.L. A cleavage cocktail for methionine-containing peptides. J. Pept. Res. 1999, 53, 548–553. [CrossRef]
27. Di, L. Strategic approaches to optimizing peptide ADME properties. Aaps. J. 2015, 17, 134–143. [CrossRef]
28. Woodley, J.F. Enzymatic barriers for GI peptide and protein delivery. Crit. Rev. Drug Carr. Syst. 1994, 11, 61–95.
29. Abdel-Hamid, M.; Otte, J.; De Gobba, C.; Osman, A.; Hamad, E. Angiotensin I-converting enzyme inhibitory activity and antioxidant capacity of bioactive peptides derived from enzymatic hydrolysis of buffalo milk proteins. Int. Dairy J. 2017, 66, 91–98. [CrossRef]
30. Shazly, A.B.; He, Z.Y.; El-Aziz, M.A.; Zeng, M.M.; Zhang, S.; Qin, F.; Chen, J. Fractionation and identification of novel antioxidant peptides from buffalo and bovine casein hydrolysates. Food Chem. 2017, 232, 753–762. [CrossRef]
31. Shazly, A.B.; Mu, H.B.; Liu, Z.M.; Aziz, M.A.; Zeng, M.M.; Qin, F.; Zhang, S.; He, Z.Y.; Chen, J. Release of antioxidant peptides from buffalo and bovine caseins: Influence of proteases on antioxidant capacities. Food Chem. 2019, 274, 261–267. [CrossRef]
32. Nakamura, Y.; Yamamoto, N.; Sakai, K.; Okubo, A.; Yamazaki, S.; Takano, T. Purification and Characterization of Angiotensin I-Converting Enzyme-Inhibitors from Sour Milk. J. Dairy Sci. 1995, 78, 777–783. [CrossRef]
33. Ariyoshi, Y. Angiotensin-Converting Enzyme-Inhibitors Derived from Food Proteins. Trends Food Sci. Tech. 1993, 4, 139–144. [CrossRef]
34. Donkor, O.N.; Henriksson, A.; Singh, T.K.; Vasiljevic, T.; Shah, N.P. ACE-inhibitory activity of probiotic yoghurt. Int. Dairy J. 2007, 17, 1321–1331. [CrossRef]
35. Papadimitriou, C.G.; Vafopoulou-Mastrojiannaki, A.; Silva, S.V.; Gomes, A.M.; Malcata, F.X.; Alichanidis, E. Identification of peptides in traditional and probiotic sheep milk yoghurt with angiotensin I-converting enzyme (ACE)-inhibitory activity. Food Chem. 2007, 105, 647–656. [CrossRef]
36. Tonouchi, H.; Suzuki, M.; Uchida, M.; Oda, M. Antihypertensive effect of an angiotensin converting enzyme inhibitory peptide from enzyme modified cheese. J. Dairy Res. 2008, 75, 284–290. [CrossRef] [PubMed]
37. Ai, L.Z.; Guo, B.H.; Zhang, H.; Wu, Z.J.; Chen, W.; Wang, Y.Y.; Tang, J.A. Isolation and antihypertensive effect of exopolysaccha-rides from Lactobacillus casei LC2W. Milchwissenschaft 2008, 63, 3–6.
38. Pepe, G.; Basilicata, M.G.; Carrizzo, A.; Adesso, S.; Ostacolo, C.; Sala, M.; Sommella, E.; Ruocco, M.; Cascioferro, S.; Ambrosio, M.; et al. beta-Lactoglobulin Heptapeptide Reduces Oxidative Stress in Intestinal Epithelial Cells and Angiotensin II-Induced Vasoconstriction on Mouse Mesenteric Arteries by Induction of Nuclear Factor Erythroid 2-Related Factor 2 (Nrf2) Translocation. Oxid. Med. Cell Longev. 2019, 2019, 1616239. [CrossRef]
39. Basilicata, M.G.; Pepe, G.; Sommella, E.; Ostacolo, C.; Manfra, M.; Sosto, G.; Pagano, G.; Novellino, E.; Campiglia, P. Peptidome profiles and bioactivity elucidation of buffalo-milk dairy products after gastrointestinal digestion. Food Res. Int. 2018, 105, 1003–1010. [CrossRef]
40. Quiros, A.; Contreras, M.D.; Ramos, M.; Amigo, L.; Recio, I. Stability to gastrointestinal enzymes and structure-activity relationship of beta-casein-peptides with antihypertensive properties. Peptides 2009, 30, 1848–1853. [CrossRef]
41. Carrizzo, A.; Vecchione, C.; Damato, A.; di Nonno, F.; Ambrosio, M.; Pompeo, F.; Cappello, E.; Capocci, L.; Peruzzi, M.; Valenti, V.; et al. Rac1 Pharmacological Inhibition Rescues Human Endothelial Dysfunction. J. Am. Heart Assoc. 2017, 6, e004746. [CrossRef]
42. Gaspari, T.A.; Vinh, A.; Jones, E.S.; Widdop, R.E. Ganging up on Angiotensin II Type 1 Receptors in Vascular Remodeling. Hypertension 2012, 60, 17–19. [CrossRef]
43. Xu, J.A.; Carretero, O.A.; Liao, T.D.; Peng, H.M.; Shesely, E.G.; Xu, J.X.; Liu, T.S.; Yang, J.J.; Reudelhuber, T.L.; Yang, X.P. Local angiotensin II aggravates cardiac remodeling in hypertension. Am. J. Physiol. Heart 2010, 299, H1328–H1338. [CrossRef] [PubMed]
44. Zhou, M.S.; Adam, A.; Raij, L. Interaction among angiotensin II, nitric oxide and oxidative stress. J. Renin Angiotensin Aldosterone Syst. 2001, 2, S59–S63. [CrossRef]
45. Forte, M.; Conti, V.; Damato, A.; Ambrosio, M.; Puca, A.A.; Sciarretta, S.; Frati, G.; Vecchione, C.; Carrizzo, A. Targeting Nitric Oxide with Natural Derived Compounds as a Therapeutic Strategy in Vascular Diseases. Oxid Med. Cell Longev. 2016, 2016, 7364138. [CrossRef] [PubMed]
46. Chakrabarti, S.; Guha, S.; Majumder, K. Food-Derived Bioactive Peptides in Human Health: Challenges and Opportunities. Nutrients 2018, 10, 1738. [CrossRef] [PubMed]
47. Carey, R.M.; Muntner, P.; Bosworth, H.B.; Whelton, P.K. Prevention and Control of Hypertension JACC Health Promotion Serie. J. Am. Coll Cardiol 2018, 72, 2996–3011. [CrossRef]
48. Baumann, M.; Sollinger, D.; Roos, M.; Lutz, J.; Heemann, U. Prehypertensive Preconditioning Improves Adult Antihypertensive and Cardioprotective Treatment. J. Pharm. Exp. 2010, 332, 1121–1126. [CrossRef]
49. McNiece, K.L.; Poffenbarger, T.S.; Turner, J.L.; Franco, K.D.; Sorof, J.M.; Portman, R.J. Prevalence of hypertension and pre-hypertension among adolescents. J. Pediatr. 2007, 150, 640–644. [CrossRef]
50. Julius, S.; Nesbitt, S.; Egan, B.; Kaciroti, N.; Schork, M.A.; Grozinski, M.; Michelson, E.; Grp, T.S. Trial of Preventing Hypertension-Design and 2-year progress report. Hypertension 2004, 44, 146–151. [CrossRef]
51. Kaplan, N.M. Trial of Preventing Hypertension (TROPHY)-Design and 2-year progress report. Hypertension 2004, 44, 125–126. [CrossRef] [PubMed]
52. Meltzer, J.I. A specialist in clinical hypertension critiques the trophy trial. Am. J. Hypertens. 2006, 19, 1098–1100. [CrossRef] [PubMed]